ObjectiveTo evaluate the effectiveness and the safety of percutaneous endoscopic gastrostomy (PEG) as compared with a nasogastric (NG) tube for adults with prolonged neurological dysphagia after stroke.DesignA prospective case-controlled study.Patients and methodsThis study included 90 patients with severe neurogenic dysphagia categorized into two groups: those on PEG feeding and those on NG feeding because they refused PEG. A comparison of both groups was assessed by several methods. The primary outcome measures were death and aspiration pneumonia during 3 months' observation and the 2ry outcome measures were changes in the nutritional state during this period and patient and family satisfaction.ResultsWeight gain was significantly higher among patients in the NG group. The incidence of aspiration pneumonia was significantly higher among patients in the NG group (14) compared with seven patients in PEG. There were four (8.3%) deaths in the PEG group compared with eight (18.2%) in the NG group.ConclusionThis study has demonstrated that PEG feeding in long-term dysphagic patients with stroke is associated with a significant reduction in the incidence of aspiration pneumonia with reduced mortality at 3 months. PEG is more acceptable and less irritating to patients and is superior in the delivery of feed and maintaining the nutritional status and improves the long-term quality of life.

Dysphagia after stroke is thought to occur in up to 45% of all strokes, compounding the problem of malnutrition and aspiration [1] . Gastrointestinal access in the short term, for up to 4-6 weeks, is usually achieved through nasogastric tubes (NGTs). If enteral feeding is likely to be needed for periods of more than 6 weeks, most international guidelines recommend a feeding gastrostomy [2] . Gastrostomy tubes are commonly inserted by percutaneous endoscopic gastrostomy (PEG) [3] .

Insertion of an NGT is easy, quick, relatively noninvasive, requires little training, and has a negligible mortality; however, many patients find NGTs uncomfortable and repeatedly pull the tube out, resulting in interrupted feeding and the potential for aspiration and malnutrition [4] . In contrast, PEG requires an invasive procedure, which can be complicated by bleeding, peritonitis, or perforation. PEG may be associated with chest infections, local infection around the insertion site, and tubes being pulled out. However, PEG is less irritating and more cosmetically acceptable to patients; PEG also appears to lead to superior feeding with respect to weight maintenance and the nutritional status, at least in patients with long-term neurogenic dysphagia [5] .

According to Potack and Chokhavatia [6] , there is a high demand for PEG in patients with swallowing disorders, with 160 000 to 200 000 PEG procedures performed per year in the USA. This makes PEG the procedure of choice for nutritional support in adults. The same author commented that many such procedures are performed, although there is no consistent evidence about what is the more effective and safe method. Because NGT and PEG are the most commonly used methods for feeding access [7] , the relative merits of PEG and NGT have been investigated. [5-9] However, it remains unclear whether PEG is superior to NGT feeding in patients with prolonged dysphagia secondary to stroke.

Objectives

To evaluate the effectiveness and the safety of PEG as compared with a NGT for adults with prolonged neurological dysphagia after stroke.

Patients and methods

A total of 90 patients with severe neurogenic dysphagia as diagnosed by clinical and fibro-optic endoscopic evaluation of swallowing (FEES) were recruited in the study. FEES was performed at the start of the study and it was based on standardized diagnostic criteria, including the presence/absence of reflex cough after swallow tests with different food consistencies and the degree of dysphagia with a validated eight-point aspiration-penetration scale (APS) [10] . The APS is an ordinal measure of dysphagia severity and airway compromise (total score 1-8, where 8 is the worst level of swallowing and 1 is the normal, safe swallow). Penetration occurs when material enters the laryngeal area to the level of the true vocal folds, whereas aspiration occurs when material moves below the true vocal folds and enters the trachea [10],[11] .

The selection criteria for inclusion were as follows: poststroke longstanding (>4 weeks) neurogenic dysphagia and a high risk of aspiration as indicated by FEES. All these patients were on nasogastric (NG) feeding for at least 4 weeks and were indicated for PEG according to NICE guidelines 2006 [12] . Detailed information and explanation of the procedures were given to the patient and his/her family by the clinician, and consent was obtained to accept PEG or refuse it. Patients were categorized into two groups: those on PEG feeding and those on NG feeding because they refused PEG. Randomization was not performed on ethical bases.

The following patient data were recorded: age and sex, the cause of dysphagia and its duration before the study, comorbidity associated with stroke, communication, and cognitive impairment. A comparison of the treatment efficacy of both groups was assessed by several methods. The primary outcome measures were death and aspiration pneumonia during 3 months' observation and the 2ry outcome measures were changes in the nutritional state during this period and patient and family satisfaction.

The following outcome measures were assessed during the 3-month follow-up period:

The absolute weight and weight change, the BMI, and its change before and at the end of the follow-up period.

The complication rate such as dislodgement, pain, infection, treatment failure, and any others.

Evidence of aspiration pneumonia during the follow-up period. Chest infection was diagnosed by the treating physician using standardized criteria (Mann criteria pneumonia) [13] based on the presence of three or more of the following variables: fever (≥38°C), productive cough with purulent sputum, abnormal respiratory examination (tachypnea, ≥22/min), tachycardia, inspiratory crackles, bronchial breathing), an abnormal chest radiograph, arterial hypoxemia (PO 2 , 70 mmHg), and isolation of a relevant pathogen (positive Gram stain and culture) [13],[14] .

Patient or family satisfaction was assessed using the modified Quality of Life (QoL) questionnaire [15] .

The number of deaths during the 3-month observation period was noted.

Statistical analysis

Descriptive statistics (median, range, count, and percentage) on patient baseline characteristics and modified QoL assessments have been calculated. Comparisons between the two feeding tubes have been made using the Mann-Whitney test for continuous variables and the Kruskal-Wallis test, Fisher's exact test, or Pearson's χ2 -test for categorical data, as appropriate. The level of significance was a P value less than 0.05.

Ethics

The Institutional Review Board (IRB) at Dubai Health Authority approved the protocol of this study and written informed consent was obtained.

Results

A total of 104 patients were recruited in the study; 14 patients were excluded as 10 shifted from NG to PEG during the follow-up period and four patients refused enteral feeding. The studied patients were classified into two groups: the PEG group included 48 patients (31 men, 17 women; mean age 78 years) and the NG group included 42 patients (26 men, 16 women; mean age 81 years).

About 83 patients had computed tomography or MRI of the brain to confirm the diagnosis of stroke, but in all cases, a firm diagnosis could be made on clinical grounds.

Assessment with FEES did not show a significant difference in the APS, and the two groups scored a mean value of more than 5 at the time of recruitment.

[Table 1] and [Table 2] show a comparison of both groups in their initial and outcome measures. No significant difference was found between both groups regarding the initial data such as age, sex, weight, and the penetration aspiration scale as assessed by FEES. The number of patients with cognitive and language impairment was higher in the PEG group, but it did not reach a significant level. Weight gain was significantly higher among patients in the PEG group compared with patients in NG (P = 0.043). The incidence of aspiration pneumonia was significantly higher among patients in the NG group [14] compared with seven patients in PEG (P = 0.029).

There were 20 patients in the NGT group who experienced feeding tube dislodgement and none in the PEG group (P = 0.0001). The median number of NGT dislodgements was two, with a range of 1-9.

Three patients in the PEG group developed a peristomal infection that resolved with antibiotics and continuation of feeding. All other gastrostomy placements were without complications. There were no treatment failures in the gastrostomy-fed group, but nine in the NG-fed group (inability to resite the NGT in three patients and recurrent removal of the tube in six patients). This difference was highly significant (P = 0.004)

There were four (8.3%) deaths in the PEG group compared with eight (18.2%) in the NG group. Analysis of the cause of death (either aspiration pneumonia or other causes) revealed that two deaths in the PEG group were due to aspiration pneumonia compared with six in the NG group. The χ2 analysis demonstrated a significantly higher mortality at 3 months in the NG group than PEG, both in the overall mortality and the aspiration-related mortality (P < 0.05).

The modified QoL questionnaire was completed within 1 month after the study onset or before discharge from the hospital. [Table 4] shows that the pain associated with the tube was worse in the PEG group than in NGT, but it did not reach a significant level (P = 0.06), whereas more patients with NGT felt that they experienced an altered body image (P = 0.05) and significantly more inconvenience than the PEG tube (P = 0.02). Nevertheless, no significant difference was found between the NGT and the PEG groups in uncomfortable feeds, learning to use, the overall physical condition, and the overall QoL.

PEG was first described by Gauderer et al.[16] as an effective method of enteral feeding through the stomach in situations where oral intake was not possible. Nowadays, PEG is a widely accepted procedure for long-term enteral feeding. The most common indication for PEG tube placement is neurologic dysphagia, which mostly develops secondary to stroke [16],[17],[18] . However, it remains unclear whether PEG is superior to NGT feeding in patients with dysphagia secondary to stroke. Jaffar et al.[19] in their systematic review study found improved mortality and nutritional outcomes with PEG feeding, but firm conclusions could not be derived on whether PEG feeding is beneficial over NG feeding in older persons with nonstroke dysphagia as previously published literature was unclear or had a high risk of bias.

The present study investigated the differences between the two methods in different aspects included the nutritional status, patients' QoL, morbidity, and mortality outcome measures. This study showed that PEG tube feeding is superior to NGT feeding for enteral nutritional support of patients with persisting dysphagia resulting from stroke. The greater weight gain in the PEG group was attributable to the greater dietary intake during uninterrupted feeding, whereas NG patients repeatedly pull out the tube resulting in the interruption of feeding and subsequent worsening of their nutritional state. The study showed that the PEG feeding group had a better QoL as patients reported a less altered body image and inconvenience than the NG group. Previous studies demonstrated similar finding, but a significantly higher incidence of pain was associated with gastrostomy tubes in the first week of insertion, whereas in our study, the pain was assessed after 1 month where pain became less severe. Previous studies found that patients in the PFG group had an advantage in terms of the cosmesis, the mobility, and the global QoL, compared with patients in the NGT group [20],[21],[22],[23] .

Many of patients with neurological dysphagia are unable to swallow their own saliva and are prone to aspiration pneumonia. Park et al.[24] in an earlier study reported that gastrostomy tube feeding does not protect one against aspiration pneumonia. Cogen and Weinryb [25] found that a history of aspiration pneumonia was the only risk factor associated with subsequent episodes during gastrostomy feeding: the age, the mental status, the type of liquid diet, or the infusion time did not affect the risk of aspiration pneumonia.

The higher incidence of aspiration pneumonia in the NG group in the present study indicated the protective role of PEG in the prevention of aspiration pneumonia. This may be related to the greater risk of pulmonary aspiration on the recurrent removal and resiting of the NGT as elderly patients do not always tolerate NG feeding and self-extubation is common, which requires frequent reintubations and close nursing surveillance [24] . In contrast, there were no instances of inadvertent removal of a gastrostomy tube. NGT may lower the esophageal sphincter pressure and increase the risk of gastroesophageal reflux with consequent aspiration [7],[26] . Another explanation for the increased risk of aspiration pneumonia in the NG group is the higher prevalence of oropharyngeal colonization by pathogenic organisms [27] .

The most striking difference was in the mortality, and the study showed that PEG feeding produced a significant reduction in the mortality at 3 months. The final recorded cause of death in 75% of the patients in the NG-fed group was bronchopneumonia, which had a higher prevalence than in the PEG group. The difference in mortality is probably a reflection of the superiority of gastrostomy feeding over NG feeding in prolonged dysphagic stroke. Several studies found that a major cause of death after a dysphagic stroke is bronchopneumonia and have shown that enteral tube feeding is associated with an increased risk of pulmonary aspiration and pneumonia, which under these conditions has a mortality of over 50% [4],[20],[24] .

An additional possible explanation for the increased mortality in the NG group was the characteristics of the NG group as it was the group that refused PEG. Lin and colleagues found that the most common reasons for refusing to use PEG were 'too old to suffer from an operation' and 'to keep individuals' body integrity,' which may reflect the more impaired patients in the NG group than in the PEG selected group. Patients who are already severely ill who are then deprived of adequate nutrition are much more likely than well-nourished patients to develop complications and have a reduced survival rate [28],[29],[30],[31] .

Conclusion

This study has demonstrated that PEG feeding in long-term dysphagic patients with stroke is associated with a significant reduction in the incidence of aspiration pneumonia with reduced mortality at 3 months. PEG is more acceptable and less irritating to patients and is superior in the delivery of feed and in maintaining the nutritional status and improves the long-term QoL.

Gomes F, Hookway C, Weekes CE. Royal College of Physicians Intercollegiate Stroke Working Party evidence-based guidelines for the nutritional support of patients who have had a stroke. J Hum Nutr Diet 2014; 27 :107-121.

Bjordal K, Ahlner-Elmqvist M, Tollesson E, Jensen AB, Razavi D, Maher EJ, Kaasa S, et al. Development of a European Organization for Research and Treatment of Cancer (EORTC) questionnaire module to be used in quality of life assessments in head and neck cancer. Acta Oncol 1994; 33 :879-885.